Characterization of neurotrophin and Trk receptor functions in developing sensory ganglia: Direct NT-3 activation of TrkB neurons in vivo

Neuron

Volumn 21, Issue 2, 1998, Pages 325-334

  Fariñas, Isabel ^a,b   Wilkinson, George A ^a,c   Backus, Carey ^a   Reichardt, Louis F ^a   Patapoutian, Ardem ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF VALENCIA   (Spain)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; NERVE GROWTH FACTOR; NEUROTROPHIN 3; NEUROTROPHIN 4; NEUROTROPHIN RECEPTOR; TYROSINE KINASE RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SUBPOPULATION; CELL SURVIVAL; EMBRYO; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SENSORY GANGLION; SPINAL GANGLION;

EID: 0032143396     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80542-5     Document Type: Article

References (42)

1. Acheson, A., Conover, J.C., Fandl, J.P., DeChiara, T.M., Russell, M., Thadani, A., Squinto, S.P., Yancopoulous, G.D., and Lindsay, R.M. (1995). A BDNF autocrine loop in adult sensory neurons prevents cell death. Nature 374, 450-453.
2. Airaksinen, M.S., Koltzenburg, M., Lewin, G.R., Masu, Y., Helbig, C., Wolf, E., Brem, G., Toyka, K.V., Thoenen, H.,and Meyer, M. (1996). Specific subtypes of cutaneous mechanoreceptors require neurotrophin-3 following peripheral target innervation. Neuron 16, 287-295.
3. Alexiades, M.R., and Cepko, C.L. (1997). Subsets of retinal progenitors display temporally regulated and distinct biases in the fates of their progeny. Development 124, 1119-1131.
4. Bamji, S.X., Madjan, M., Pozniak, C.D., Belliveau, D.J., Alyz, R., Kohn, J., Causing, C.G., and Miller, F.D. (1998). The p75 neurotrophin receptor mediates neuronal apoptosis and is essential for naturally occurring sympathetic neuron death. J. Cell Biol. 140, 911-927.
5. Clary, D.O., Weskamp, G., Austin, L.A.R., and Reichardt, L.F. (1994). TrkA cross-linking mimics neuronal responses to nerve growth factor. Mol. Biol. Cell 5, 549-563.
6. Crowley, C., Spencer, S.D., Nishimura, M.C., Chen, K.S., Pitts-Meek, S., Armanini, M.P., Ling, G.H., McMahon, S.B., Shelton, D.L., Levinson, A.D., and Phillips, H.S. (1994). Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76, 1001-1011.
7. Davies, A.M., Bandtlow, C.E., Heumann, R., Korsching, S., Rohrer, H., and Thoenen, H. (1987). Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. Nature 326, 353-357.
8. Davies, A.M., Minichiello, L., and Klein, R. (1995). Developmental changes in NT3 signaling via TrkA and TrkB in embryonic neurons. EMBO J. 14, 4482-4489.
9. ElShamy, W.M., and Ernfors, P. (1996). A local action of neurotrophin-3 prevents the death of proliferating sensory neuron precursor cells. Neuron 16, 963-972.
10. Ernfors, P., Lee, K.F., Kucera, J., and Jaenisch, R. (1994). Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell 77, 503-512.
11. Fariñas, I., Jones, K.R., Backus, C., Wang, X.-Y., and Reichardt, L.F. (1994). Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature 369, 658-661.
12. Fariñas, I., Yoshida, C.K., Backus, C., and Reichardt, L.F. (1996). Lack of neurotrophin-3 results in death of spinal sensory neurons and premature differentiation of their precursors. Neuron 17, 1065-1078.
13. Gaese, F., Kolbeck, R., and Barde, Y.A. (1994). Sensory ganglia require neurotrophin-3 in early development. Development 120, 1613-1619.
14. Haddon, C., Smithers, L., Schneider-Maunoury, S., Coche, T., Henrique, D., and Lewis, J. (1998). Multiple delta genes and lateral inhibition in zebrafish primary neurogenesis. Development 125, 359-370.
15. Henion, P.D., Garner, A.S., Large, T.H., and Weston, J.A. (1995). TrkC-mediated NT-3 signaling is required for the early development of a subpopulation of neurogenic neural crest cells. Dev. Biol. 172, 602-613.
16. Ip, N.Y., Stitt, T.N., Tapley, P., Klein, R., Glass, D.J., Fandl, J., Greene, L.A., Barbacid, M., and Yancopoulos, G.D. (1993). Similarities and differences in the way neurotrophins interact with the Trk receptors in neuronal and nonneuronal cells. Neuron 10, 137-149.
17. Kalcheim, C., Carmeli, C., and Rosenthal, A. (1992). Neurotrophin-3 is a mitogen for cultured neural crest cells. Proc. Natl. Acad. Sci. USA 89, 1661-1665.
18. Klein, R., Martín-Zanca, D., Barbacid, M., and Parada, L.F. (1990). Expression of the tyrosine kinase receptor gene trkB is confined to the murine embryonic and adult nervous system. Development 109, 845-850.
19. Klein, R., Smeyne, R.J., Wurst, W., Long, L.K., Auerbach, B.A., Joyner, A.L., and Barbacid, M. (1993). Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesions and neonatal death. Cell 75, 113-122.
20. Klein, R., Silos-Santiago, I., Smeyne, R.J., Lira, S.A., Brambilla, R., Bryant, S., Zhang, L., Snider, W.D., and Barbacid, M. (1994). Disruption of the neurotrophin-3 receptor gene trkC eliminates la muscle afferents and results in abnormal movements. Nature 368, 249-251.
21. Lamballe, F., Smeyne, R., and Barbacid, M. (1994). Developmental expression of TrkC, the neurotrophin-3 receptor, in the mammalian nervous system. J. Neurosci. 14, 14-28.
22. Lefcort, F., Clary, D.O., Rusoff, A.C., and Reichardt, L.F. (1996). Inhibition of the NT-3 receptor TrkC, early in chick embryogenesis, results in severe reductions in multiple neuronal subpopulations in the dorsal root ganglia. J. Neurosci. 16, 3704-3713.
23. Liebl, D.J., Tessarollo, L., Palko, M.E., and Parada, L.F. (1997). Absence of sensory neurons before target innervation in brain-derived neurotrophic factor-, neurotrophin-3-, and TrkC-deficient embryonic mice. J. Neurosci. 17, 9113-9121.
24. Martin, S.C., Sandell, J.H., and Heinrich, G. (1998). Zebrafish TrkC1 and TrkC2 receptors define two different cell populations in the nervous system during the period of axonogenesis. Dev. Biol. 195, 114-130.
25. Martín-Zanca, D., Barbacid, M., and Parada, L.F. (1990). Expression of the trk protooncogene is restricted to the sensory cranial and spinal ganglia of neural crest origin in mouse development. Genes Dev. 4, 683-694.
26. McMahon, S.B., Armanini, M.P., Ling, L.H., and Phillips, H.S. (1994). Expression and coexpression of trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 12, 1161-1171.
27. Memberg, S.P., and Hall, A.K. (1995). Proliferation, differentiation, and survival of rat sensory neuron precursors in vitro require specific trophic factors. Mol. Cell. Neurosci. 6, 323-335.
28. Minichiello, L., Piehl, F., Vazquez, E., Schimmang, T., Hokfelt, T., Represa, J., and Klein, R. (1995). Differential effects of combined Trk receptor mutations on dorsal root ganglion and inner ear sensory neurons. Development 121, 4067-4075.
29. Reichardt, L.F., and Fariñas, I. (1997). Neurotrophic factors and their receptors: roles in neuronal development and function. In Molecular Approaches to Neural Development, M.W. Cowan, T.M. Jessell, and L. Zipurski, eds. (New York: Oxford University Press), pp. 220-263.
30. Schecterson, L.C., and Bothwell, M. (1992). Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons. Neuron 9, 449-463.
31. Scott, S.A. (1992). Sensory Neurons: Diversity, Development, and Plasticity. (New York: Oxford University Press).
32. Sieber-Blum, M. (1991). Role of the neurotrophic factors BDNF and NGF in the commitment of pluripotent neural crest cells. Neuron 6, 949-955.
33. Silos-Santiago, I., Molliver, D.C., Ozaki, S., Smeyne, R.J., Fagan, A.M., Barbacid, M., and Snider, W.D. (1995). Non-TrkA-expressing small DRG neurons are lost in TrkA-deficient mice. J. Neurosci. 15, 5929-5942.
34. Silos-Santiago, I., Fagan, A.M., Garber, M., Fritzsch, B., and Barbacid, M. (1997). Severe sensory deficits but normal CNS development in newborn mice lacking TrkB and TrkC tyrosine protein kinase receptors. Eur. J. Neurosci. 9, 2045-2056.
35. Smeyne, R.J., Klein, R., Schnapp, A., Long, L.K., Bryant, S., Lewin, A., Lira, S.A., and Barbacid, M. (1994). Severe sensory and sympathetic neuropathies in mice carrying a disrupted trk/NGF receptor gene. Nature 368, 246-248.
36. Tessarollo, L., Tsoulfas, P., Martín-Zanca, D., Gilbert, D.J., Jenkins, N.A., Copeland, N.G., and Parada, L.F. (1993). TrkC, a receptor for neurotrophin-3, is widely expressed in the developing nervous system and in nonneuronal tissues. Development 118, 463-475.
37. Tessarollo, L., Vogel, K.S., Palko, M.E., Reid, S.W., and Parada, L.F. (1994). Targeted mutation in the neurotrophin-3 gene results in loss of muscle sensory neurons. Proc. Natl. Acad. Sci. USA 91, 11844-11848.
38. Tessarollo, L., Tsoulfas, P., Donovan, M.J., Palko, M.E., Blair-Flynn, J., Hempstead, B.L., and Parada, L.F. (1997). Targeted deletion of all isoforms of the trkC gene suggests the use of alternate receptors by its ligand neurotrophin-3 in neuronal development and implicates TrkC in normal cardiogenesis. Proc. Natl. Acad. Sci. USA 94, 14776-14781.
39. Tojo, H., Kaisho, Y., Nakata, M., Matsuoka, K., Kitagawa, M., Abe, T., Takami, K., Yamamoto, M., Shino, A., Igarashi, K., et al. (1995). Targeted disruption of the neurotrophin-3 gene with lacZ induces loss of TrkC-positive neurons in sensory ganglia but not in spinal cords. Brain Res. 669, 163-175.
40. Weskamp, G., and Reichardt, L.F. (1991). Evidence that biological activity of NGF is mediated through a novel subclass of high affinity receptors. Neuron 6, 649-663.
41. White, F.A., Silos-Santiago, I., Molliver, D.C., Nishimura, M., Phillips, H., Barbacid, M., and Snider, W.D. (1996). Synchronous onset of NGF and TrkA survival dependence in developing dorsal root ganglia. J. Neurosci. 16, 4662-4672.
42. Wilkinson, G.A (1997). Neurotrophin-3 and Trk receptors in the developing mouse trigeminal ganglion. PhD thesis, University of California, San Francisco, CA, pp. 1-163.